Cerebrum

Synaptic Self: How Our Brains Become Who We Are

Joseph LeDoux’s second book for lay readers, Synaptic Self: How Our Brains Become Who We Are, is about the neurobiological underpinnings of...you. After a brief survey of arcane philosophical concepts of self, LeDoux slashes the Gordian knot: “My notion of personality is pretty simple: it’s that your ‘self,’ the essence of who you are, reﬂects patterns of interconnectivity between neurons in your brain.” The meat of the book is a systematic, thoughtful, and erudite defense of that opening manifesto. In his conclusion, LeDoux’s parting words resonate with the beginning like a well-chosen rhyme: “You are your synapses. They are who you are.”

A 21ST-CENTURY MYTH

This straightforward pronouncement, so uncontroversial—even axiomatic—to most neuroscientists, will likely have the force of eye-opening revelation to many a lay reader, even a highly cultured one. By making his point in a thoughtful and readable fashion, LeDoux seeks to rid the general public of some of its most entrenched cultural misconceptions. Whether or not he will succeed is a different question.

Redeﬁning C. P. Snow’s famous phrase, the author and literary personality John Brockman refers to “the third culture”—a recent and still emerging intellectual environment characterized by the convergence of two social phenomena. The notion of “intelligentsia” has undergone a gradual transformation as we have come to recognize that, in forming a cultured mind, grasping fundamental scientiﬁc concepts is as important as being familiar with the humanities. Sensing that transformation, some notable scientists are redeﬁning their proper contribution to culture. They decline to be anonymous puppeteers of social development, relating to the general public only as consumers who are removed from the scientist’s intellectual work. They are descending from their ivory towers to communicate with people directly and personally, bringing an authority that no journalist, no professional popularizer, can command.

Thus we see a spate of highbrow popular books about the brain. But Synaptic Self is different. LeDoux does not stake out a delimited terrain of neuroscience, dutifully mapping it in lay language; he sets out to popularize cognitive neuroscience as a whole. As a professor at the Center for Neural Science at New York University, with prestigious research awards from the National Institute of Mental Health, the National Science Foundation, and other sources, he is duly qualiﬁed for the job.

It is not a small task, however, to debunk the widely held belief that the soul exists apart from the brain.

It is not a small task, however, to debunk the widely held belief that the soul exists apart from the brain. Just how entrenched is the notion, even among the most educated, that our selves, our personalities, are somehow extra-cranial? Recently I participated in a symposium occasioned by the Olympic Games. The topic was “What Makes a Champion?” Although linked with a particular athletic event, the symposium’s purpose was broad: to unravel the secrets of extraordinary success in human endeavors. A few dozen luminaries from different walks of life spoke: political leaders, captains of industry, past Olympic champions, Nobel scientists, legendary explorers, and cultural personalities. I felt privileged and humbled to ﬁnd myself in their company.

As the discussion unfolded, a dominant theme emerged. Virtually without exception, even repetitively, speakers maintained that great success rests on two foundations. One is a special, domain-speciﬁc ability, a talent without which success is impossible, no matter how hard one tries. But, to ensure achievement at the champion level, that specialized talent must be complemented by another, equally indispensable ingredient: a particular personality type. The champion personality, said the speakers, is distinguished by drive, ambition, persistence, and the ability to subordinate trivial urges to a lofty long-term goal, to delay gratiﬁcation.

As I listened to these speakers, I sensed the ghost of René Descartes in the great convention hall. The specialized talent was biological destiny—some exceptional attribute of body and brain—but the champion spirit was conceived in oddly extracranial terms, like an aura or a stew of Puritan virtue and free will.

When my turn came, I said that personality, spirit, soul—whatever you want to call it—is also of the brain. Human variation in attributes like drive, capacity for delayed gratiﬁcation, and sustained focus to a large extent reﬂects variations in individual neurobiological attributes. As I was warming to this subject, I was suddenly rebuffed by a fellow panelist, a famous diplomat. “What you are saying, Professor Goldberg, is very interesting,” he interjected, “but this conference is not about the brain. It is about the mind.” I sensed no hint of a doubt that he knew what he was talking about.

I think that my jaw dropped in disbelief. I had to make a split-second decision: pick a ﬁght or let it go? Considerations of civility instructed me to let it go. But the encounter is etched in my memory, a striking reminder of the spell cast by the delusion of body-soul duality, cast over even the most enlightened members of the general public at the dawn of the 21st century. As I read LeDoux’s new book, I found myself wishing that I could have handed out copies at that meeting as a parting gift to my fellow panelists.

FROM MOLECULE TO CULTURE

Think of Synaptic Self as an introductory textbook on cognitive neuroscience for the educated person, one free of the stylistic bombast, stiffness, and Germanic turn of phrase endemic in standard textbooks. Written in the first person, it resembles a textbook nevertheless in its panoramic sweep from molecular neuroscience to cognitive neuroscience. LeDoux may take exception to this definition, because his book is also about philosophy, psychology, and sociology. Unlike most trade books about brain science, which are narrower, more focused, Synaptic Self says something about nearly everything pertaining to neuroscience.

With few exceptions, it tackles these matters in a marvelously accessible way. A spectrum of readers will ﬁnd it useful. The generally cultured but neuroscientiﬁcally uninitiated reader, one of our proverbial intelligentsia, will ﬁnd in Synaptic Self a wealth of ideas and facts about the brain presented in an inviting yet sophisticated fashion. The educated lay reader interested in psychology will ﬁnd a compelling, articulate, and spirited defense of mind as the product of brain. The advanced student of neuroscience, not needing such convincing, will find a cogent, state-of-the-art review of a panorama of brain topics. The undergraduate student may use it as a primer. Not least, the busy clinician, like myself, aware of the neuroscience fundamentals but spotty about certain of the latest neuroscience findings, will seize on it as a fine, up-to-date refresher. Even the most initiated reader, a fellow neuroscientist, should feel as I did: Most of the facts and ideas are familiar, but revisiting them proves highly enjoyable because LeDoux writes so well.

He has a rare combination of expertise, style, and wit, a synaptic self that comes across well and agreeably in his writing.

LeDoux’s writing is idiosyncratic in a way that entertains and enlivens. I feel afﬁnity for scientists who do not hesitate to project their personalities into their writings—and have a personality to project. So I was delighted to ﬁnd LeDoux guiding us through the maze of synaptic arborization and then the no less enticing maze of New Orleans’s French Quarter. He has a rare combination of expertise, style, and wit, a synaptic self that comes across well and agreeably in his writing.

The book’s rendering of the biological underpinnings of the mind is generally uncontroversial, probably by intent. LeDoux gives us a balanced, evenhanded account of the current consensus about brain mechanisms. There are no extreme positions, and I found nothing with which to take exception, nothing into which to sink my polemical teeth, had I been so inclined. Indeed, freedom from controversy is the book’s strength, what its purpose requires. For a prolific scientist active in the intellectual arena to refrain from polemical thrust and parry is an act of self-discipline.

Mind you, LeDoux presents some high-proﬁle controversies: nature vs. nurture, instructionism vs. selectionism, and nativism vs. behaviorism. But in every case he reviews the pros and cons in a measured, dispassionate way, and usually reaches a middle-of-the-road conclusion, preferring conjunction to disjunction.

LeDoux is underwhelmed by the mystery of consciousness. He dethrones it from its customary status as the central question of cognitive neuroscience, which is especially corrective for the general reader.

LeDoux is underwhelmed by the mystery of consciousness. He dethrones it from its customary status as the central question of cognitive neuroscience, which is especially corrective for the general reader because popular renditions of neuroscience so often over-emphasize consciousness. To me, it seems anomalous that philosophers and psychologists devote 90 percent of their own intellectual horsepower to unraveling mysteries that account for 10 percent (probably less) of our mental life at any given time. Neglect of the unconscious mental processes that we run on autopilot, and that account for a far greater portion of our mental life, has distorted psychology and artificially narrowed its scope. LeDoux articulates this problem passionately and convincingly at the outset. He then takes us on a well-planned trip through the history of philosophical thought on the subject of consciousness, particularly within the Cartesian paradigm, which equates cognition with consciousness—and thus unduly restricts the scope of inquiry into the nature of the mind and sets the stage for much conceptual trouble.

A welcome aspect of Synaptic Self is the volley of eclectic, freewheeling, but broadly relevant digressions that LeDoux lets loose.

A welcome aspect of Synaptic Self is the volley of eclectic, freewheeling, but broadly relevant digressions that LeDoux lets loose. He stirs in vignettes from philosophy, theology, and history, betokening his diverse interests and intellectual conﬁdence. After all, the third culture is broad and its avenues are two-way. Just as humanists are often, and often self-righteously, ignorant of the sciences, so the technocrats of science are often dismissive of insights from the humanities. In contrast to such intellectual tunnel vision, LeDoux’s synthesis across domains is refreshing.

THE LAYERS OF SELF

Synaptic Self has eleven chapters in a basically bottom-up sequence. In the first six, LeDoux provides us with a tour de force through morphogenesis; neural plasticity and learning; neurotransmitters and neuromodulators; cortical and hippocampal mechanisms of implicit and explicit memory and amnesias; the amygdala and fear conditioning with its “low” (thalamic) and “high” (cortical) roads; and the synaptic mechanisms of learning. The hero is the synapse.

This sets the stage for ﬁve chapters that tackle the mental trilogy of cognition, emotion, and motivation. First is a brief, somewhat derivative review of the basics of the executive functions of the frontal lobes and the ubiquitous role of working memory; of the dorsolateral cortex and consciousness; and of the role of language in cognition. Then comes a review of the studies of emotion, where LeDoux is an acknowledged master. His ﬁrst book for the layman, The Emotional Brain: The Mysterious Underpinnings of Emotional Life (Simon & Schuster, 1996), focused entirely on the emotions, including his own seminal research. In Synaptic Self, he addresses the problem of credibility inherent in any study of subjective states via externally observable behavior, proposes ways of circumventing it, and discusses the possibility of emotional experiences in other species.

We find a cogent critique of the limbic system as a Humpty Dumpty with little glue to keep it together. This is followed by discussion of the role of the amygdala in generating the response to fear, the hippocampus in processing the context of the fear-triggering event, the medial frontal regions in moderating the fear response, and recent functional neuroimaging studies aimed at elucidating the human brain’s fear circuitry. LeDoux emphasizes that, despite cortical imperialism, the “low” thalamic road to the amygdala still appears to be the main road to fear. A lucid discussion follows of the relationship between the formation of memories and moderate arousal (which helps memory formation), in contrast to stress (which hurts it).

What of the mechanisms of “fear itself”? LeDoux relates fear to the amygdala’s flooding, monopolizing virtually all cognition, from the early stages of sensory processing to the integrative regions of the frontal lobes. As if to keep his narrative from becoming too morbid, LeDoux interjects a speculative discussion of the neurobiology of love, presenting a singularly monogamous rodent, the prairie vole, as a model of attachment to its mate that is mediated by vasopressin and oxytocin. He does not, however, discuss what makes this faithful rodent more monogamous than we humans.

LeDoux deﬁnes emotions as “the process by which the brain determines or computes the value of the stimulus.” Because it explicitly bridges emotional, motivational, and cognitive aspects of decision making (pointing to the blurry nature of the very distinction), this is a deﬁnition rich with possibilities. It resonates strongly with what I term “actor-centered” (what is good for me?), as opposed to “veridical” (what is the objective truth?), decision making, linked strongly to the frontal lobes. I wish LeDoux had explored the theme at greater length.

The third part of the mental trilogy is motivation and the mechanisms by which the emotion system affects incentive-driven behavior. Somewhat in passing, LeDoux makes a distinction between emotional (incentive-driven) behavior and emotional feelings—the former not necessarily requiring the latter. This claim is crucial, because it further bridges cognition, emotion, and motivation. The role of dopamine and the frontal lobes in motivated behavior is then discussed.

The chapter next reviews social-psychological theories of motivation and concludes with an admonition difﬁcult to dispute:

A mind is not, as cognitive science has traditionally suggested, just a thinking device. It’s an integrated system that includes, in the broadest possible terms, synaptic networks devoted to cognitive, emotional, and motivational functions. More important, it involves interactions between networks involved in different aspects of mental life....Consciousness is important, but so are the underlying cognitive, emotional, and motivational processes that work unconsciously.

There follows a review of major psychiatric disorders, which LeDoux judiciously limits to schizophrenia, depression and its relationship to stress, anxiety, the role of genes in psychiatric disorders, and the relative roles of pharmacology and therapy in the treatment of non-psychotic disorders. He argues that the mechanisms of these diseases are best understood not in terms of molecules but in terms of circuits, as complex connections and interactions among the prefrontal cortex, hippocampus, amygdala, and ventral brainstem. He offers interesting, albeit unproven, speculation on the neuroanatomical loci of action (all involving some kind of interaction between the prefrontal cortex and the amygdala) of various forms of psychotherapy.

While most of this ﬂows seamlessly, almost effortlessly, certain chapters of necessity are more dense and technical. An example is the discussion of glutamate receptors in synaptic transmission, synaptic plasticity, second messengers, retrograde messengers, protein kinases, neurotropins, and other elements of the biochemical machinery of learning and memory.

LeDoux interleaves his discussion of state-of-the-art neuroscience with vignettes from the history of science: the neuronal versus reticular controversy of the late nineteenth century; the intellectual precursors of the Hebbian learning model; the pains of birth of the synaptic theory of learning; the more recent use by Eric Kandel and his associates of Aplysia californica as a model for the basic mechanisms of memory and learning; and false starts and serendipities in the discovery of psychotropic drugs.

Particularly appealing in Synaptic Self is the back-and-forth between basic science and practical issues of therapy. An important phenomenon studied in LeDoux’s lab has been new or additional synthesis of protein that occurs after a memory has been accessed in a particular new context. This phenomenon, known as “memory reconsolidation,” is the age of molecular biology’s answer to Bartlett’s famous insight that remembering is always an active process of reconfiguration. Once a memory has been called up, used in a new context, it is no longer its own exact self; additional biochemical processes have attended its integration into a changed network of associations. Indeed, without such additional protein synthesis, a memory accessed is a memory lost. This seemingly technical discovery is ripe with clinical implications and real-life dilemmas that LeDoux does not fail to entertain. Can you erase an unwanted memory by interfering with protein synthesis while reliving the memory before your mind’s eye? What will sanitation of memory do to a person’s identity? These interesting digressions go far toward making even the denser parts of Synaptic Self captivating for the uninitiated reader.

I take exception to a few points in the book: a somewhat mechanistic rendition of memory “transfer” from structure to structure (particularly dangerous in a popular book, since a relatively naive reader is likely to take it literally and picture a little axonal pushcart loaded with memories); the obligatory role of consciousness in memory encoding (how about incidental learning?); hippocampal damage being necessary for the failure of conscious retrieval (how about the strictly neocortical aphasia interfering with a conscious retrieval of a lexical item?), to mention a few. But dwelling on these exceptions would miss the point of LeDoux’s book and of this review.

If self is all-embracing, must not Synaptic Self in some sense be all-embracing? Perhaps so, and this gives the book an impressively encyclopedic quality.

SEVEN PRINCIPLES OF ASSEMBLING THE SELF

If self is all-embracing, must not Synaptic Self in some sense be all-embracing? Perhaps so, and this gives the book an impressively encyclopedic quality, albeit one that distracts somewhat from the powerful, parsimonious message that surely was in the author’s mind. The message is certainly compelling, with the author deliberately and logically building his case to a crescendo, but the seemingly irresistible urge to address everything has a cramming effect. With more than 1,000 references, Synaptic Self is as erudite a popular review of cognitive neuroscience as one is likely to encounter. In the end, however, I suspect that the people who most need to have their minds changed will find Synaptic Self a bit over their heads—too great a mental (synaptic?) effort. It is an open question whether the general public is ready to grasp the synaptic concept of self. But, like every crusade to debunk a deeply entrenched popular conception (or misconception), the key is repetition as much as rational argument. Synaptic Self is a powerful and important voice in that extended process.

EXCERPT

The study of learning and memory processes in the brain has advanced rapidly in the last few decades. This book is in large part based upon this new understanding of encoding and storage and their origin in synaptic function. Learning, and its synaptic result, memory, play major roles in gluing a coherent personality together as one goes through life. Without learning and memory processes, personality would be merely an empty, impoverished expression of our genetic constitution. Learning allows us to transcend our genes, or, as the novelist Salman Rushdie said, “Life teaches us who we are.” Our genes may bias the way we act, but the systems responsible for much of what we do and how we do it are shaped by learning. Although a rat is by nature afraid of cats, it will live longer if it learns where in its particular world cats are most likely to be encountered and what kinds of sounds and smells are present when cats are nearby. A rat that has stored this information in its fear system is more worldly, and much better off, than one that has not. Something similar occurs in many if not most other brain systems: the information they encode and store today will contribute importantly to how they function tomorrow...

But, as we will see throughout this book, learning and memory also contribute to personality in ways that exceed explicit self-knowledge. The brain, in other words, learns and stores many things in networks that function outside of conscious awareness. These learned tendencies affect all aspects of mind and behavior, and are probably at least as important for day-to-day functioning as what we know about ourselves consciously.

My walk down Bourbon Street got me thinking about the origins of the self as the key overarching problem that neuroscience should aim to solve. Many other brain scientists, however, might be inclined to say that consciousness is the big one.

Neuroscientists traditionally have avoided confronting consciousness. The topic was one that retired neuroscientists, facing their own mortality, would talk about, but young brain researchers knew better. Even joking about it could give you a bad reputation. But times have changed and discussions of consciousness by neuroscientists are on the rise....

I think it’s good that scientists are now interested in consciousness, but I also believe it’s being overemphasized. Suppose next week we find out that after decades of false starts and failed promises, an indefatigable neuroscientist finally has solved the consciousness problem. Would that really tell us what makes people tick? Would we now understand why schizophrenia emerges in one person but not his twin brother; why, when two people are faced with bodily harm, one is paralyzed by his fear while the other fights back; why an excessively shy child is likely to become an anxious adult; why some people are vegetarians and others enjoy red meat; why my kids can’t stand the music I listen to; or why I like theirs? The answer to each of these is clearly No!

The question Synaptic Self asks is not “How does consciousness come out of the brain?” but rather “How does our brain make us who we are?”

What a person is, and what he or she thinks, feels, and does, is by no stretch of the imagination influenced only by consciousness. Many of our thoughts, feelings, and actions take place automatically, with consciousness only coming to know them as they happen, if at all. Figuring out the mechanism of consciousness would surely be a major scientific coup, but it wouldn’t explain how the brain works, or how our brains make us the individuals we are.

An understanding of the mystery of personality crucially depends on figuring out the unconscious functions of the brain...

We can be and often are aware of what we are doing when these things happen, but much of the time consciousness is informed after the fact. When someone speaks to you, for example, you decode sentence meaning on the basis of the sound of the words (phonology), the meaning of the words (semantics), the grammatical relations between the words (syntax), and your knowledge about the world (pragmatics). You usually are not aware of performing these operations, but simply do them. While you end up consciously knowing what the person said, you don’t have conscious access to the processes that allowed you to comprehend the sentence. Similarly, when you yourself utter sentences, you go through the same processes, often without a conscious thought, but this time as the generator rather than the receiver. Our abilities to perceive the world, attend to objects and events, remember, imagine, and think all operate pretty much in this fashion. Collectively, these processes have been called the psychological or cognitive unconscious, and they account for much of mental life.

Does that mean we’ll know what a person is when we figure out the operations of these various conscious and unconscious functions? While unlocking the synaptic mechanisms underlying each of these processes is itself going to be quite a challenge, we need to go beyond the mere explanation of how each works in isolation. We need to understand how the many processes interact, and how the particular interactions that take place inside an individual’s brain give rise to and maintain who he or she is. My aim in this book is to show how it is possible, at least in principle, to begin to understand the self in terms of such synaptic interactions.

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Bill Glovin, editor Carolyn Asbury, Ph.D., consultant

Scientific Advisory Board Joseph T. Coyle, M.D., Harvard Medical School Kay Redfield Jamison, Ph.D., The Johns Hopkins University School of Medicine Pierre J. Magistretti, M.D., Ph.D., University of Lausanne Medical School and Hospital Robert Malenka, M.D., Ph.D., Stanford University School of Medicine Bruce S. McEwen, Ph.D., The Rockefeller University Donald Price, M.D., The Johns Hopkins University School of Medicine